Biometals

, Volume 8, Issue 4, pp 339–351

Expression of metallothionein genes during the post-embryonic development of Drosophila melanogaster

  • Michèle Durliat
  • François Bonneton
  • Elisabeth Boissonneau
  • Michèle André
  • Maurice Wegnez
Article

Abstract

Expression of the two Drosophila melanogaster metallothionein genes, Mtn and Mto, has been analyzed by in situ hybridization during post-embryonic development. Mtn and Mto transcripts were detected exclusively in the digestive tract of larvae, pupae and adults reared on standard medium. Mtn and Mto expression domains overlap, but each gene is also expressed at unique sites. Mtn mRNA levels are approximately 10 and 20 times higher than those of Mto in larvae and adults, respectively. Copper and cadmium ions strongly induce Mtn and Mto mRNA accumulation in the midgut. Zinc is a weaker inducer, acting only at high concentrations. Mtn gene expression is induced by these three metals in Malpighian tubules, while Mto gene expression in this organ is induced only by zinc. Iron is a poor inducer of metallothionein mRNA accumulation. Functions of MTN and MTO proteins in metal homeostasis and detoxification are considered.

Keywords

metallothionein development metal induction Drosophila 

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References

  1. Andrews GK, Huet-Hudson YM, Paria BC, McMaster MT, De SK, Dey SK. 1991 Metallothionein gene expression and metal regulation during preimplantation mouse embryo development. Der Biol 145, 13–27.Google Scholar
  2. Beach LR, Palmiter RD. 1981 Amplification of the metallothionein-I gene in cadmium-resistant mouse cells. Proc Natl Acad Sci USA 78, 2110–2114.Google Scholar
  3. Bonneton F, Wegnez M. 1995 Developmental variability of metallothionein Mtn gene expression in the species of the Drosophila melanogaster subgroup. Dev Genet 16, 253–263.Google Scholar
  4. Bouquegneau JM, Ballan-Dufrançais C, Jeantet AY. 1985 Storage of Hg in the ileum of Blatella germanica: biochemical characterization of metallothionein. Comp Biochem Physiol 80C, 95–98.Google Scholar
  5. Bryant PJ, Levinson P. 1985 Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of the lethal mutation causing overgrowth. Dev Biol 107, 355–363.Google Scholar
  6. Carlson JR, Hogness DS. 1985 Developmental and functional analysis of Jonah gene expression. Dev Biol 108, 355–368.Google Scholar
  7. Debec A, Mokdad R, Wegnez M. 1985 Metallothioneins and resistance to cadmium poisoning in Drosophila cells. Biochem Biophys Res Commun 127, 143–152.Google Scholar
  8. Dimitriadis VK, Kastritsis CD. 1984 Ultrastructural analysis of the midgut of Drosophila auraria larvae. Morphological observations and their physiological implications. Can J Zool 62, 659–669.Google Scholar
  9. Erraïss NE, Silar P, Cadic-Jacquier A, Modkad-Gargouri R, Wegnez M. 1989 The metallothionein system of Drosophila melanogaster. In: Hamer DH, Winge DR, eds. Metal Ion Homeostasis: Molecular Biology and Chemistry. New York: Alan R Liss; 91–99.Google Scholar
  10. Filshie BK, Poulson DF, Waterhouse DF. 1971 Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 3, 77–102.Google Scholar
  11. Hamer DH. 1986 Metallothionein. Annu Rev Biochem 55, 913–951.Google Scholar
  12. Karin M. 1985 Metallothioneins: proteins in search of function. Cell 41, 9–10.Google Scholar
  13. Lange BW, Langley CH,Stephan W. 1990 Molecular evolution of Drosophila metallothionein genes. Genetics 126, 921–932.Google Scholar
  14. Lastowski-Perry D, Otto E, Maroni G. 1985 Nucleotide sequence and expression of a Drosophila metallothionein. J Biol Chem 260, 1527–1530.Google Scholar
  15. Lauverjat S, Ballan-Dufrançais C, Wegnez M. 1989 Detoxification of cadmium. Ultrastructural study and electron-probe microanalysis of the midgut in a cadmium-resistant strain of Drosophila melanogaster. Biol Metals 2, 97–107.Google Scholar
  16. Marchal-Ségault D, Briançon C, Halpern S, Fragu P, Laugé G. 1990 Secondary ion mass spectrometry analysis of the copper distribution in Drosophila melanogaster chronically intoxicated with Bordeaux mixture. Biol Cell 70, 129–132.Google Scholar
  17. Maroni G. 1989 Animal metallothioneins. In: Shaw AJ, ed. Heavy Metal Tolerance in Plants. Boca Raton: CRC Press; 215–232.Google Scholar
  18. Maroni G. Watson D. 1985 Uptake and binding of cadmium, copper and zinc by Drosophila melanogaster larvae. Insect Biochem 15, 55–63.Google Scholar
  19. Maroni G, Otto E, Lastowski-Perry D. 1986 Molecular and cytogenetic characterization of a metallothionein gene of Drosophila. Genetics 112, 493–504.Google Scholar
  20. Maroni G, Wise J, Young JE, Otto E. 1987 Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117, 739–744.Google Scholar
  21. Masters BA, Kelly EJ, Quaife CJ, Brinster RL,Palmiter RD. 1994 Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc Natl Acad Sci USA 91, 584–588.Google Scholar
  22. Mastrippolito R, Bendali M, Charon Y, Leblanc M, Martin B, Tricoire H, Valentin L. 1991 SOFI: a bidimensional detector for fast direct on-line quantification of beta particles on blots. Bio Techniques 11, 778–783.Google Scholar
  23. McCormick CC. 1984 The tissue-specific accumulation of hepatic zinc metallothionein following parenteral iron loading. Proc Soc Exp Biol Med 176, 392–402.Google Scholar
  24. Michalska AE, Choo KHA. 1993 Targeting and germ-line transmission of a null mutation at the metallothionein I and II loci in mouse. Proc Natl Acad Sci USA 90, 8088–8092.Google Scholar
  25. Miller A. 1965 The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M, ed. Biology of Drosophila. New York: Hafner: 420–534.Google Scholar
  26. Mokdad R, Debec A, Wegnez M. 1987 Metallothionein genes in Drosophila melanogaster constitute a dual system. Proc Natl Acad Sci USA 84, 2658–2662.Google Scholar
  27. Nemer M, Thornton RD, Stuebing EW, Harlow P. 1991 Structure, spatial, and temporal expression of two sea urchin metallothionein genes, SpMTB1 and SpMTA. J Biol Chem 266, 6586–6593.Google Scholar
  28. Otto E, Young JE, Maroni G. 1986 Structure and expression of a tandem duplication of the Drosophila metallothionein gene. Proc Natl Acad Sci USA 83, 6025–6029.Google Scholar
  29. Poulson DF, Bowen VT. 1952 Organization and function of the inorganic constituents of nuclei. Exp Cell Res. Suppl 2, 161–179.Google Scholar
  30. Poulson DF, Bowen VT, Hilse RM, Rubinson AC. 1952 The copper metabolism of Drosophila. Proc Natl Acad Sci USA 38, 912–921.Google Scholar
  31. Price D, Joshi JG. 1982 Ferritin: a zinc detoxicant and a zinc ion donor. Proc Natl Acad Sci USA 79, 3116–3119.Google Scholar
  32. Price DJ, Joshi JG. 1983 Ferritin-binding of beryllium and other divalent metal ions. J Biol Chem 258, 10873–10880.Google Scholar
  33. Richards MP. 1989 Recent developments in trace element metabolism and function: role of metallothionein in copper and zinc metabolism. J Nutr 119, 1062–1070.Google Scholar
  34. Sato M, Bremner I. 1993 Oxygen free radicals and metallothionein. Free Rad Biol Med 14, 325–337.Google Scholar
  35. Silar P, Théodore L, Mokdad R, Erraïss NE, Cadic A, Wegnez M. 1990 Metallothionein Mto gene of Drosophila melanogaster: Structure and regulation J Mol Biol 215, 217–224.Google Scholar
  36. Sohal RS, Lamb RE, 1979 Storage-excretion of metallic cations in the adult housefly, Musca domestica. J Insect Physiol 25, 119–124.Google Scholar
  37. Sohal RS, Peters PD, Hall TA. 1976 Fine structure and X-ray microanalysis of mineralized concretions in the Malpighian tubules of the housefly, Musca domestica. Tissue Cell 8, 447–458.Google Scholar
  38. Tamai KT, Gralla EB, Ellerby LM, Valentine JS, Thiele DJ. 1993 Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 90, 8013–8017.Google Scholar
  39. Tapp RL, Hockaday A. 1977 Combined histochemical and X-ray microanalytical studies on the copper-accumulating granules in the mid-gut of larval Drosophila. J Cell Sci 26, 201–215.Google Scholar
  40. Terra WR, Espinoza-Fuentes FP, Ribeiro AF, Ferreira C. 1988 The larval midgut of the housefly (Musca domestica): ultrastructure, fluid fluxes and ion secretion in relation to the organization of digestion. J Insect Physiol 34, 463–472.Google Scholar
  41. Théodore E, Ho AS, Maroni G. 1991 Recent evolutionary history of the metallothionein gene Mtn in Drosophila. Genet Res Camb 58, 203–210.Google Scholar
  42. Tsuji S, Kobayashi H, Uchida Y, Ihara Y, Miyatake T. 1992 Molecular cloning of human growth inhibitory factor cDNA and its down-regulation in Alzheimer's disease. EMBO J 11, 4843–4850.Google Scholar
  43. Uchida Y, Takio K, Titani K, Ihara Y, Tomonaga M. 1991 The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Neuron 7, 337–347.Google Scholar
  44. Wessing A, Eichelberg D. 1978 Malpighian tubules, rectal papillae and excretion. In: Ashburner M, Wright TRF, eds. The Genetics and Biology oj Drosophila. London: Academic Press; 2C, 1–42.Google Scholar
  45. Zierold K, Wessing A. 1990 Mass dense vacuoles in Drosophila Malpighian tubules contain zinc, not sodium. A reinvestigation by X-ray microanalysis of cryosections. Eur J Cell Biol 53, 222–226.Google Scholar

Copyright information

© Rapid Science Publishers 1995

Authors and Affiliations

  • Michèle Durliat
    • 1
  • François Bonneton
    • 1
  • Elisabeth Boissonneau
    • 1
  • Michèle André
    • 1
  • Maurice Wegnez
    • 1
  1. 1.Laboratoire Emhryologie Moléculaire et Expérimentale, URA 1134 du CNRS, Université Paris XIOrsayFrance
  2. 2.Laboratoire d'Embryologie Moléculaire et Expérimentale, Université Parix XIOrsayFrance

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